Cross-tolerance and Cross-talk in the Cold: Relating Low Temperatures to Desiccation and Immune Stress in Insects

Sinclair, Brent J.; Ferguson, Laura V.; Salehipourshirazi, Golnaz; MacMillan, Heath A.

doi:10.1093/icb/ict004

Cited by 241 publications

(264 citation statements)

References 88 publications

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“…Broadly, work on short-term cold shock gene expression changes has shown that the predominant group of genes showing expression changes are those involved in the stress and immune response (e.g. heat shock proteins (Hsps), Turandot genes, etc) (Zhang et al, 2011;Sinclair et al, 2013;Storey and Storey, 2013). In addition, the neuropeptide CAPA has been shown to play an important role in both cold and desiccation resistance in several species of Drosophila, including D. montana, when assessed using cold shock (Terhzaz et al, submitted).…”

Section: Functional Processesmentioning

confidence: 99%

How consistent are the transcriptome changes associated with cold acclimation in two species of the Drosophila virilis group?

et al. 2015

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For many organisms the ability to cold acclimate with the onset of seasonal cold has major implications for their fitness. In insects, where this ability is widespread, the physiological changes associated with increased cold tolerance have been well studied. Despite this, little work has been done to trace changes in gene expression during cold acclimation that lead to an increase in cold tolerance. We used an RNA-Seq approach to investigate this in two species of the Drosophila virilis group. We found that the majority of genes that are differentially expressed during cold acclimation differ between the two species. Despite this, the biological processes associated with the differentially expressed genes were broadly similar in the two species. These included: metabolism, cell membrane composition, and circadian rhythms, which are largely consistent with previous work on cold acclimation/cold tolerance. In addition, we also found evidence of the involvement of the rhodopsin pathway in cold acclimation, a pathway that has been recently linked to thermotaxis. Interestingly, we found no evidence of differential expression of stress genes implying that long-term cold acclimation and short-term stress response may have a different physiological basis.

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Section: Functional Processesmentioning

confidence: 99%

How consistent are the transcriptome changes associated with cold acclimation in two species of the Drosophila virilis group?

et al. 2015

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“…Exposure to a particular stressor might enhance tolerance to a subsequent stress if the physiological protective mechanisms against the two stressors are shared (cross-tolerance, e.g. Elnitsky et al, 2009;Holmstrup et al, 2002) or, conversely, can cause the organisms to be more susceptible to the second stress (cross-susceptibility) (Sinclair et al, 2013;Todgham and Stillman, 2013).…”

Section: Introductionmentioning

confidence: 99%

Aquatic insects in a multistress environment: cross-tolerance to salinity and desiccation

Pallarés

Botella‐Cruz

Arribas

et al. 2017

Journal of Experimental Biology

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Exposing organisms to a particular stressor may enhance tolerance to a subsequent stress, when protective mechanisms against the two stressors are shared. Such cross-tolerance is a common adaptive response in dynamic multivariate environments and often indicates potential co-evolution of stress traits. Many aquatic insects in inland saline waters from Mediterranean-climate regions are sequentially challenged with salinity and desiccation stress. Thus, cross-tolerance to these physiologically similar stressors could have been positively selected in insects of these regions. We used adults of the saline water beetles Enochrus jesusarribasi (Hydrophilidae) and Nebrioporus baeticus (Dytiscidae) to test cross-tolerance responses to desiccation and salinity. In independent laboratory experiments, we evaluated the effects of (i) salinity stress on the subsequent resistance to desiccation and (ii) desiccation stress (rapid and slow dehydration) on the subsequent tolerance to salinity. Survival, water loss and haemolymph osmolality were measured. Exposure to stressful salinity improved water control under subsequent desiccation stress in both species, with a clear cross-tolerance (enhanced performance) in N. baeticus. In contrast, general negative effects on performance were found under the inverse stress sequence. The rapid and slow dehydration produced different water loss and haemolymph osmolality dynamics that were reflected in different survival patterns. Our finding of cross-tolerance to salinity and desiccation in ecologically similar species from distant lineages, together with parallel responses between salinity and thermal stress previously found in several aquatic taxa, highlights the central role of adaption to salinity and co-occurring stressors in arid inland waters, having important implications for the species' persistence under climate change.

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“…Both cold and desiccation stress result in decreased hemolymph volume and increased hemolymph osmolarity (4), so it is reasonable to expect mechanistic overlap between these stresses. Indeed, similar molecular mechanisms, including calcium signaling pathways, appear to modulate cold and desiccation responses (5,6). Several studies have shown that freezetolerant insects can improve their cold tolerance in response to a mild desiccation stress (7)(8)(9), and artificial selection for desiccation tolerance in Drosophila melanogaster impacts the ability to recover from chill coma (10).…”

mentioning

confidence: 99%

Insect capa neuropeptides impact desiccation and cold tolerance

Terhzaz

Teets

Cabrero

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

107

128

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The success of insects is linked to their impressive tolerance to environmental stress, but little is known about how such responses are mediated by the neuroendocrine system. Here we show that the capability (capa) neuropeptide gene is a desiccation-and cold stressresponsive gene in diverse dipteran species. Using targeted in vivo gene silencing, physiological manipulations, stress-tolerance assays, and rationally designed neuropeptide analogs, we demonstrate that the Drosophila melanogaster capa neuropeptide gene and its encoded peptides alter desiccation and cold tolerance. Knockdown of the capa gene increases desiccation tolerance but lengthens chill coma recovery time, and injection of capa peptide analogs can reverse both phenotypes. Immunohistochemical staining suggests that capa accumulates in the capa-expressing Va neurons during desiccation and nonlethal cold stress but is not released until recovery from each stress. Our results also suggest that regulation of cellular ion and water homeostasis mediated by capa peptide signaling in the insect Malpighian (renal) tubules is a key physiological mechanism during recovery from desiccation and cold stress. This work augments our understanding of how stress tolerance is mediated by neuroendocrine signaling and illustrates the use of rationally designed peptide analogs as agents for disrupting protective stress tolerance.environmental stress | insects | neuropeptides | capa | desiccation and cold tolerance

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Cross-tolerance and Cross-talk in the Cold: Relating Low Temperatures to Desiccation and Immune Stress in Insects

Cited by 241 publications

References 88 publications

How consistent are the transcriptome changes associated with cold acclimation in two species of the Drosophila virilis group?

How consistent are the transcriptome changes associated with cold acclimation in two species of the Drosophila virilis group?

Aquatic insects in a multistress environment: cross-tolerance to salinity and desiccation

Insect capa neuropeptides impact desiccation and cold tolerance

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